Viruses in bats and potential spillover to animals and humans

Current Opinion in Virology

Volumn 34, Issue , 2019, Pages 79-89

  Wang, Lin Fa ^a   Anderson, Danielle E ^a  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BAT; CORONAVIRINAE; DISEASE SEVERITY; FILOVIRUS; HUMAN; INFECTION RISK; NONHUMAN; PARAMYXOVIRIDAE; PRIORITY JOURNAL; REOVIRIDAE; REVIEW; RISK ASSESSMENT; RNA VIRUS; RNA VIRUS INFECTION; VIRUS TRANSMISSION; ANIMAL; COMMUNICABLE DISEASE; DISEASE CARRIER; EPIDEMIC; GENETICS; HENDRA VIRUS; PATHOGENICITY; SARS CORONAVIRUS; VETERINARY MEDICINE; VIROLOGY; VIRUS; VIRUS INFECTION; ZOONOSIS;

ANIMALS; CHIROPTERA; COMMUNICABLE DISEASES, EMERGING; CORONAVIRUS; DISEASE OUTBREAKS; DISEASE RESERVOIRS; HENDRA VIRUS; HUMANS; SARS VIRUS; VIRUS DISEASES; VIRUSES; ZOONOSES;

EID: 85060110949     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2018.12.007     Document Type: Review

References (138)

1. Taylor, L.H., Latham, S.M., Woolhouse, M.E., Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 356 (2001), 983–989.
2. Allen, T., Murray, K.A., Zambrana-Torrelio, C., Morse, S.S., Rondinini, C., Di Marco, M., Breit, N., Olival, K.J., Daszak, P., Global hotspots and correlates of emerging zoonotic diseases. Nat Commun, 8, 2017, 1124 An updated version of the 2008 publication (Ref. [3]) with better modeling data and updated maps, which is an important resource for assessing risk of future emerging zoonotic diseases.
3. Jones, K.E., Patel, N.G., Levy, M.A., Storeygard, A., Balk, D., Gittleman, J.L., Daszak, P., Global trends in emerging infectious diseases. Nature 451 (2008), 990–993.
4. Bean, A.G., Baker, M.L., Stewart, C.R., Cowled, C., Deffrasnes, C., Wang, L.F., Lowenthal, J.W., Studying immunity to zoonotic diseases in the natural host - keeping it real. Nat Rev Immunol 13 (2013), 851–861.
5. Calisher, C.H., Childs, J.E., Field, H.E., Holmes, K.V., Schountz, T., Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev 19 (2006), 531–545 Although it has been a decade since its publication, this paper remains to be one of the best reviews on this subject.
6. Olival, K.J., Hosseini, P.R., Zambrana-Torrelio, C., Ross, N., Bogich, T.L., Daszak, P., Host and viral traits predict zoonotic spillover from mammals. Nature 546 (2017), 646–650 A milestone paper demonstrating the special status of bats as virus reservoir.
7. Wong, S., Lau, S., Woo, P., Yuen, K.Y., Bats as a continuing source of emerging infections in humans. Rev Med Virol 17 (2007), 67–91.
8. Wang, L.F., Walker, P.J., Poon, L.L., Mass extinctions, biodiversity and mitochondrial function: are bats’ special’ as reservoirs for emerging viruses?. Curr Opin Virol 1 (2011), 649–657.
9. Luis, A.D., Hayman, D.T., O'Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R., Mills, J.N., Timonin, M.E., Willis, C.K., Cunningham, A.A., et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?. Proc Biol Sci, 280, 2013 20122753.
10. Teeling, E.C., Springer, M.S., Madsen, O., Bates, P., O'Brien, S.J., Murphy, W.J., A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307 (2005), 580–584.
11. Teeling, E.C., Vernes, S.C., Davalos, L.M., Ray, D.A., Gilbert, M.T.P., Myers, E., Bat biology, genomes, and the Bat1K project: to generate chromosome-level genomes for all living bat species. Annu Rev Anim Biosci 6 (2018), 23–46.
12. Smith, I., Wang, L.F., Bats and their virome: an important source of emerging viruses capable of infecting humans. Curr Opin Virol 3 (2013), 84–91.
13. Peiris, J.S., Yuen, K.Y., Osterhaus, A.D., Stohr, K., The severe acute respiratory syndrome. N Engl J Med 349 (2003), 2431–2441.
14. Wang, L.F., Eaton, B.T., Bats, civets and the emergence of SARS. Curr Top Microbiol Immunol 315 (2007), 325–344.
15. Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J.H., Wang, H., Crameri, G., Hu, Z., Zhang, H., et al. Bats are natural reservoirs of SARS-like coronaviruses. Science 310 (2005), 676–679.
16. Lau, S.K., Woo, P.C., Li, K.S., Huang, Y., Tsoi, H.W., Wong, B.H., Wong, S.S., Leung, S.Y., Chan, K.H., Yuen, K.Y., Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102 (2005), 14040–14045.
17. Hu, D., Zhu, C., Ai, L., He, T., Wang, Y., Ye, F., Yang, L., Ding, C., Zhu, X., Lv, R., et al. Genomic characterization and infectivity of a novel SARS-like coronavirus in Chinese bats. Emerg Microbes Infect, 7, 2018, 154.
18. Ge, X.Y., Li, J.L., Yang, X.L., Chmura, A.A., Zhu, G., Epstein, J.H., Mazet, J.K., Hu, B., Zhang, W., Peng, C., et al. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 28 (2013), 535–538 After more than ten years of continuous investigation, this paper finally demonstrated bats as the true reservoir of SARS related viruses.
19. Menachery, V.D., Yount, B.L., Sims, A.C., Debbink, K., Agnihothram, S.S., Gralinski, L.E., Graham, R.L., Scobey, T., Plante, J.A., Royal, S.R., et al. SARS-like WIV1-CoV poised for human emergence. Proc Nat Acad Sci 113 (2016), 3048–3053.
20. Zaki, A.M., van Boheemen, S., Bestebroer, T.M., Osterhaus, A.D., Fouchier, R.A., Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367 (2012), 1814–1820 The paper opened a whole new area of MERS research, which is not going to stop in the foreseeable future.
21. Middle East respiratory syndrome coronavirus (MERS-CoV) on World Wide Web URL: http://www.who.int/emergencies/mers-cov/en/.
22. Reusken, C.B., Haagmans, B.L., Muller, M.A., Gutierrez, C., Godeke, G.J., Meyer, B., Muth, D., Raj, V.S., Smits-De Vries, L., Corman, V.M., et al. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect Dis 13 (2013), 859–866.
23. Azhar, E.I., El-Kafrawy, S.A., Farraj, S.A., Hassan, A.M., Al-Saeed, M.S., Hashem, A.M., Madani, T.A., Evidence for camel-to-human transmission of MERS coronavirus. N Engl J Med 370 (2014), 2499–2505.
24. Haagmans, B.L., Al Dhahiry, S.H., Reusken, C.B., Raj, V.S., Galiano, M., Myers, R., Godeke, G.J., Jonges, M., Farag, E., Diab, A., et al. Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect Dis 14 (2014), 140–145 An important finding indicating that camels are the reservoir or amplifying host of MERS-CoV in Middle East.
25. Chu, D.K., Poon, L.L., Gomaa, M.M., Shehata, M.M., Perera, R.A., Abu Zeid, D., El Rifay, A.S., Siu, L.Y., Guan, Y., Webby, R.J., et al. MERS coronaviruses in dromedary camels, Egypt. Emerg Infect Dis 20 (2014), 1049–1053.
26. Muller, M.A., Meyer, B., Corman, V.M., Al-Masri, M., Turkestani, A., Ritz, D., Sieberg, A., Aldabbagh, S., Bosch, B.J., Lattwein, E., et al. Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis 15 (2015), 559–564.
27. Sabir, J.S.M., Lam, T.T.-Y., Ahmed, M.M.M., Li, L., Shen, Y.E.M., Abo-Aba, S., Qureshi, M.I., Abu-Zeid, M., Zhang, Y., Khiyami, M.A., et al. Co-circulation of three camel coronavirus species and recombination of MERS-CoVs in Saudi Arabia. Science 351 (2016), 81–84 It is important to find that MERS-CoV is not the only CoV circulating in Middle East camals.
28. Ithete, N.L., Stoffberg, S., Corman, V.M., Cottontail, V.M., Richards, L.R., Schoeman, M.C., Drosten, C., Drexler, J.F., Preiser, W., Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg Infect Dis 19 (2013), 1697–1699.
29. Luo, C.-M., Wang, N., Yang, X.-L., Liu, H.-Z., Zhang, W., Li, B., Hu, B., Peng, C., Geng, Q.-B., Zhu, G.-J., et al. Discovery of novel bat coronaviruses in South China that use the same receptor as Middle East respiratory syndrome coronavirus. J Virol, 92, 2018.
30. Anthony, S.J., Gilardi, K., Menachery, V.D., Goldstein, T., Ssebide, B., Mbabazi, R., Navarrete-Macias, I., Liang, E., Wells, H., Hicks, A., et al. Further evidence for bats as the evolutionary source of Middle East respiratory syndrome coronavirus. mBio, 8, 2017 An important finding although the evidence is not very strong.
31. Tao, Y., Shi, M., Chommanard, C., Queen, K., Zhang, J., Markotter, W., Kuzmin, I.V., Holmes, E.C., Tong, S., Surveillance of bat coronaviruses in Kenya identifies relatives of human coronaviruses NL63 and 229E and their recombination history. J Virol, 91, 2017.
32. Zhou, P., Fan, H., Lan, T., Yang, X.L., Shi, W.F., Zhang, W., Zhu, Y., Zhang, Y.W., Xie, Q.M., Mani, S., et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556 (2018), 255–258 This paper highlights that lethal outbreaks by bat CoVs are not limited to humans, they can happen in livestock animals as well.
33. Murray, K., Selleck, P., Hooper, P., Hyatt, A., Gould, A., Gleeson, L., Westbury, H., Hiley, L., Selvey, L., Rodwell, B., et al. A morbillivirus that caused fatal disease in horses and humans. Science 268 (1995), 94–97 First discovery of a bat-borne BSL4 virus which can affect both human and animals.
34. Field, H.E., Hendra virus ecology and transmission. Curr Opin Virol 16 (2016), 120–125.
35. Summary of Hendra virus incidents in horses on World Wide Web URL: https://www.business.qld.gov.au/industries/service-industries-professionals/service-industries/veterinary-surgeons/guidelines-hendra/incident-summary.
36. Field, H., de Jong, C., Melville, D., Smith, C., Smith, I., Broos, A., Kung, Y.H., McLaughlin, A., Zeddeman, A., Hendra virus infection dynamics in Australian fruit bats. PLoS One, 6, 2011 e28678.
37. Chua, K.B., Goh, K.J., Wong, K.T., Kamarulzaman, A., Tan, P.S., Ksiazek, T.G., Zaki, S.R., Paul, G., Lam, S.K., Tan, C.T., Fatal encephalitis due to Nipah virus among pig-farmers in Malaysia [see comments]. Lancet 354 (1999), 1257–1259.
38. Chua, K.B., Bellini, W.J., Rota, P.A., Harcourt, B.H., Tamin, A., Lam, S.K., Ksiazek, T.G., Rollin, P.E., Zaki, S.R., Shieh, W., et al. Nipah virus: a recently emergent deadly paramyxovirus. Science 288 (2000), 1432–1435.
39. Hsu, V.P., Hossain, M.J., Parashar, U.D., Ali, M.M., Ksiazek, T.G., Kuzmin, I., Niezgoda, M., Rupprecht, C., Bresee, J., Breiman, R.F., Nipah virus encephalitis reemergence, Bangladesh. Emerg Infect Dis 10 (2004), 2082–2087.
40. Luby, S.P., Hossain, M.J., Gurley, E.S., Ahmed, B.N., Banu, S., Khan, S.U., Homaira, N., Rota, P.A., Rollin, P.E., Comer, J.A., et al. Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001-2007. Emerg Infect Dis 15 (2009), 1229–1235.
41. Nipah virus – India on World Wide Web URL: http://www.who.int/csr/don/07-august-2018-nipah-virus-india/en/.
42. Yob, J.M., Field, H., Rashdi, A.M., Morrissy, C., van der Heide, B., Rota, P., bin Adzhar, A., White, J., Daniels, P., Jamaluddin, A., et al. Nipah virus infection in bats (order Chiroptera) in peninsular Malaysia. Emerg Infect Dis 7 (2001), 439–441.
43. Chua, K.B., Lek Koh, C., Hooi, P.S., Wee, K.F., Khong, J.H., Chua, B.H., Chan, Y.P., Lim, M.E., Lam, S.K., Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4 (2002), 145–151.
44. Epstein, J.H., Prakash, V., Smith, C.S., Daszak, P., McLaughlin, A.B., Meehan, G., Field, H.E., Cunningham, A.A., Henipavirus infection in fruit bats (Pteropus giganteus), India. Emerg Infect Dis 14 (2008), 1309–1311.
45. Yadav, P.D., Raut, C.G., Shete, A.M., Mishra, A.C., Towner, J.S., Nichol, S.T., Mourya, D.T., Detection of Nipah virus RNA in fruit bat (Pteropus giganteus) from India. Am J Trop Med Hyg 87 (2012), 576–578.
46. Anderson, D.E., Islam, A., Crameri, G., Todd, S., Khan, S.U., Foord, A., Rahman, M.Z., Mendenhall, I.H., Luby, S.P., Gurley, E.S., et al. Isolation and full-genome characterization of Nipah viruses from bats, Bangladesh. Emerg Infect Dis, 25, 2019.
47. Marsh, G.A., de Jong, C., Barr, J.A., Tachedjian, M., Smith, C., Middleton, D., Yu, M., Todd, S., Foord, A.J., Haring, V., et al. Cedar virus: a novel Henipavirus isolated from Australian bats. PLoS Pathog, 8, 2012, e1002836.
48. Olson, J.G., Rupprecht, C., Rollin, P.E., An, U.S., Niezgoda, M., Clemins, T., Walston, J., Ksiazek, T.G., Antibodies to Nipah-like virus in bats (Pteropus lylei), Cambodia. Emerg Infect Dis 8 (2002), 987–988.
49. Sendow, I., Ratnawati, A., Taylor, T., Adjid, R.M., Saepulloh, M., Barr, J., Wong, F., Daniels, P., Field, H., Nipah virus in the fruit bat Pteropus vampyrus in Sumatera, Indonesia. PLoS One, 8, 2013 e69544.
50. Pernet, O., Schneider, B.S., Beaty, S.M., LeBreton, M., Yun, T.E., Park, A., Zachariah, T.T., Bowden, T.A., Hitchens, P., Ramirez, C.M., et al. Evidence for henipavirus spillover into human populations in Africa. Nat Commun, 5, 2014, 5342.
51. Peel, A.J., Baker, K.S., Crameri, G., Barr, J.A., Hayman, D.T., Wright, E., Broder, C.C., Fernandez-Loras, A., Fooks, A.R., Wang, L.F., et al. Henipavirus neutralising antibodies in an isolated island population of African fruit bats. PLoS One, 7, 2012, e30346.
52. Hayman, D.T., Suu-Ire, R., Breed, A.C., McEachern, J.A., Wang, L., Wood, J.L., Cunningham, A.A., Evidence of henipavirus infection in West African fruit bats. PLoS One, 3, 2008, e2739.
53. Iehle, C., Razafitrimo, G., Razainirina, J., Andriaholinirina, N., Goodman, S.M., Faure, C., Georges-Courbot, M.C., Rousset, D., Reynes, J.M., Henipavirus and Tioman virus antibodies in pteropodid bats, Madagascar. Emerg Infect Dis 13 (2007), 159–161.
54. Drexler, J.F., Corman, V.M., Muller, M.A., Maganga, G.D., Vallo, P., Binger, T., Gloza-Rausch, F., Cottontail, V.M., Rasche, A., Yordanov, S., et al. Bats host major mammalian paramyxoviruses. Nat Commun, 3, 2012, 796 A very large study demonstrating the great diversity of bat borne viruses in multiple viral families.
55. Chant, K., Chan, R., Smith, M., Dwyer, D.E., Kirkland, P., Probable human infection with a newly described virus in the family Paramyxoviridae. The NSW expert group. Emerg Infect Dis 4 (1998), 273–275.
56. Philbey, A.W., Kirkland, P.D., Ross, A.D., Field, H.E., Srivastava, M., Davis, R.J., Love, R.J., Infection with Menangle virus in flying foxes (Pteropus spp.) in Australia. Aust Vet J 86 (2008), 449–454.
57. Barr, J.A., Smith, C., Marsh, G.A., Field, H., Wang, L.F., Evidence of bat origin for Menangle virus, a zoonotic paramyxovirus first isolated from diseased pigs. J Gen Virol 93 (2012), 2590–2594.
58. Chua, K.B., Wang, L.F., Lam, S.K., Crameri, G., Yu, M., Wise, T., Boyle, D., Hyatt, A.D., Eaton, B.T., Tioman virus, a novel paramyxovirus isolated from fruit bats in Malaysia. Virology 283 (2001), 215–229.
59. Yaiw, K.C., Bingham, J., Crameri, G., Mungall, B., Hyatt, A., Yu, M., Eaton, B., Shamala, D., Wang, L.F., Thong Wong, K., Tioman virus, a paramyxovirus of bat origin, causes mild disease in pigs and has a predilection for lymphoid tissues. J Virol 82 (2008), 565–568.
60. Katoh, H., Kubota, T., Ihara, T., Maeda, K., Takeda, M., Kidokoro, M., Cross-neutralization between human and African Bat mumps viruses. Emerg Infect Dis 22 (2016), 703–706 For the first time, it is demonstrated that a mumps virus close relative exists in non-human mammals.
61. Krüger, N., Hoffmann, M., Drexler, J.F., Müller, M.A., Corman, V.M., Sauder, C., Rubin, S., He, B., Örvell, C., Drosten, C., et al. Functional properties and genetic relatedness of the fusion and hemagglutinin-neuraminidase proteins of a mumps virus-like bat virus. J Virol 89 (2015), 4539–4548.
62. Beaty, S.M., Nachbagauer, R., Hirsh, A., Vigant, F., Duehr, J., Azarm, K.D., Stelfox, A.J., Bowden, T.A., Duprex, W.P., Krammer, F., et al. Cross-reactive and cross-neutralizing activity of human mumps antibodies against a novel mumps virus from bats. J Infect Dis 215 (2017), 209–213.
63. Kruger, N., Sauder, C., Huttl, S., Papies, J., Voigt, K., Herrler, G., Hardes, K., Steinmetzer, T., Orvell, C., Drexler, J.F., et al. Entry, replication, immune evasion, and neurotoxicity of synthetically engineered bat-borne mumps virus. Cell Rep 25 (2018), 312–320 e317.
64. Stephan, H., Gay, G., Ramirez, T., Encephalomyelitis, reproductive failure and corneal opacity (blue eye) in pigs, associated with a paramyxovirus infection. Vet Rec 122 (1988), 6–10.
65. Salas-Rojas, M., Sanchez-Hernandez, C., Romero-Almaraz Md Mde, L., Schnell, G.D., Schmid, R.K., Aguilar-Setien, A., Prevalence of rabies and LPM paramyxovirus antibody in non-hematophagous bats captured in the Central Pacific coast of Mexico. Trans R Soc Trop Med Hyg 98 (2004), 577–584.
66. Wang, L.F., Hansson, E., Yu, M., Chua, K.B., Mathe, N., Crameri, G., Rima, B.K., Moreno-Lopez, J., Eaton, B.T., Full-length genome sequence and genetic relationship of two paramyxoviruses isolated from bat and pigs in the Americas. Arch Virol 152 (2007), 1259–1271.
67. Zeller, H.G., Karabatsos, N., Calisher, C.H., Digoutte, J.P., Cropp, C.B., Murphy, F.A., Shope, R.E., Electron microscopic and antigenic studies of uncharacterized viruses. II. Evidence suggesting the placement of viruses in the family Bunyaviridae. Arch Virol 108 (1989), 211–227.
68. Lau, S.K., Woo, P.C., Wong, B.H., Wong, A.Y., Tsoi, H.W., Wang, M., Lee, P., Xu, H., Poon, R.W., Guo, R., et al. Identification and complete genome analysis of three novel paramyxoviruses, tuhoko virus 1, 2 and 3, in fruit bats from China. Virology 404 (2010), 106–2116.
69. Albarino, C.G., Foltzer, M., Towner, J.S., Rowe, L.A., Campbell, S., Jaramillo, C.M., Bird, B.H., Reeder, D.M., Vodzak, M.E., Rota, P., et al. Novel paramyxovirus associated with severe acute febrile disease, South Sudan and Uganda, 2012. Emerg Infect Dis 20 (2014), 211–216 Although it was limited to a single patient, it demonstrated that the spill over events of bat viruses may occur more frequently than we expected.
70. Amman, B.R., Albarino, C.G., Bird, B.H., Nyakarahuka, L., Sealy, T.K., Balinandi, S., Schuh, A.J., Campbell, S.M., Stroher, U., Jones, M.E., et al. A recently discovered pathogenic paramyxovirus, sosuga virus, is present in rousettus aegyptiacus fruit bats at multiple locations in Uganda. J Wildl Dis 51 (2015), 774–779.
71. Piot, P., Spencer, J., From 1976 to 2018: reflections on early investigations into the Ebola virus. Trans R Soc Trop Med Hyg 112 (2018), 527–528.
72. Nakkazi, E., DR Congo ebola virus outbreak: responding in a conflict zone. Lancet, 392, 2018, 623.
73. Goldstein, T., Anthony, S.J., Gbakima, A., Bird, B.H., Bangura, J., Tremeau-Bravard, A., Belaganahalli, M.N., Wells, H.L., Dhanota, J.K., Liang, E., et al. The discovery of Bombali virus adds further support for bats as hosts of ebolaviruses. Nat Microbiol 3 (2018), 1084–1089.
74. Johnson, E.D., Johnson, B.K., Silverstein, D., Tukei, P., Geisbert, T.W., Sanchez, A.N., Jahrling, P.B., Characterization of a new Marburg virus isolated from a 1987 fatal case in Kenya. Arch Virol Suppl 11 (1996), 101–114.
75. Towner, J.S., Khristova, M.L., Sealy, T.K., Vincent, M.J., Erickson, B.R., Bawiec, D.A., Hartman, A.L., Comer, J.A., Zaki, S.R., Stroher, U., et al. Marburgvirus genomics and association with a large hemorrhagic fever outbreak in Angola. J Virol 80 (2006), 6497–6516.
76. Negredo, A., Discovery of an ebolavirus-like filovirus in Europe. PLoS Pathog, 7, 2011, e1002304.
77. Kemenesi, G., Kurucz, K., Dallos, B., Zana, B., Foldes, F., Boldogh, S., Gorfol, T., Carroll, M.W., Jakab, F., Re-emergence of Lloviu virus in Miniopterus schreibersii bats, Hungary, 2016. Emerg Microbes Infect, 7, 2018, 66.
78. Yang, X.-L., Tan, C.W., Anderson, D.E., Jian, R.-D., Li, B., Zhang, W., Zhu, Y., Lim, X.F., Zhou, P., Liu, X.-L., et al. Characterization of a filovirus (Měnglà virus) from Rousettus bats in China. Nat Microbiol, 2019, 10.1038/s41564-018-0328-y This is the first time that a novel filovirus representing a new genus is discovered in Asia.
79. Towner, J.S., Amman, B.R., Sealy, T.K., Carroll, S.A., Comer, J.A., Kemp, A., Swanepoel, R., Paddock, C.D., Balinandi, S., Khristova, M.L., et al. Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog, 5, 2009, e1000536 This is important in the context of debate on whether bats are true reservoir of filoviruses.
80. Schuh, A.J., Amman, B.R., Towner, J.S., Filoviruses and bats. Microbiol Aust 38 (2017), 12–16.
81. Leendertz, S.A.J., Testing new hypotheses regarding ebolavirus reservoirs. Viruses 8 (2016), 30–34.
82. Schiff, L.A., Nibert, M.L., Tyler, K.L., Orthoreoviruses and their replication. Knipe, D.M., Griffin, D.E., Lamb, R.A., Straus, S.E., Howley, P.M., Martin, M.A., Roizman, B., (eds.) Fields Virology, 2007, Lippincott Williams & Wilkins, 1853–1915.
83. Chua, K.B., Crameri, G., Hyatt, A., Yu, M., Tompang, M.R., Rosli, J., McEachern, J., Crameri, S., Kumarasamy, V., Eaton, B.T., et al. A previously unknown reovirus of bat origin is associated with an acute respiratory disease in humans. Proc Natl Acad Sci U S A 104 (2007), 11424–11429 First demonstration that bat reovirus can cause severe diseases in humans, which opened up a new field of research with many more discoveries of similar cases in different countries.
84. Gard, G.P., Marshall, I.D., Nelson Bay virus. A novel reovirus. Arch Gesamte Virusforsch 43 (1973), 34–42.
85. Pritchard, L.I., Chua, K.B., Cummins, D., Hyatt, A., Crameri, G., Eaton, B.T., Wang, L.F., Pulau virus; a new member of the Nelson Bay orthoreovirus species isolated from fruit bats in Malaysia. Arch Virol 151 (2006), 229–239.
86. Chua, K.B., Voon, K., Crameri, G., Tan, H.S., Rosli, J., McEachern, J.A., Suluraju, S., Yu, M., Wang, L.F., Identification and characterization of a new orthoreovirus from patients with acute respiratory infections. PLoS One, 3, 2008, e3803.
87. Cheng, P., Lau, C.S., Lai, A., Ho, E., Leung, P., Chan, F., Wong, A., Lim, W., A novel reovirus isolated from a patient with acute respiratory disease. J Clin Virol 45 (2009), 79–80.
88. Du, L., Lu, Z., Fan, Y., Meng, K., Jiang, Y., Zhu, Y., Wang, S., Gu, W., Zou, X., Tu, C., Xi river virus, a new bat reovirus isolated in southern China. Arch Virol 155 (2010), 1295–1299.
89. Chua, K.B., Voon, K., Yu, M., Keniscope, C., Abdul Rasid, K., Wang, L.F., Investigation of a potential zoonotic transmission of orthoreovirus associated with acute influenza-like illness in an adult patient. PLoS One, 6, 2011 e25434.
90. Wong, A.H., Cheng, P.K., Lai, M.Y., Leung, P.C., Wong, K.K., Lee, W.Y., Lim, W.W., Virulence potential of fusogenic orthoreoviruses. Emerg Infect Dis 18 (2012), 944–948.
91. Singh, H., Yoshikawa, T., Kobayashi, T., Fukushi, S., Tani, H., Taniguchi, S., Fukuma, A., Yang, M., Sugamata, M., Shimojima, M., et al. Rapid whole genome sequencing of Miyazaki-Bali/2007 Pteropine orthoreovirus by modified rolling circular amplification with adaptor ligation - next generation sequencing. Sci Rep, 5, 2015, 16517.
92. Hu, T., Qiu, W., He, B., Zhang, Y., Yu, J., Liang, X., Zhang, W., Chen, G., Zhang, Y., Wang, Y., et al. Characterization of a novel orthoreovirus isolated from fruit bat, China. BMC Microbiol, 14, 2014, 293.
93. Lorusso, A., Teodori, L., Leone, A., Marcacci, M., Mangone, I., Orsini, M., Capobianco-Dondona, A., Camma, C., Monaco, F., Savini, G., A new member of the Pteropine Orthoreovirus species isolated from fruit bats imported to Italy. Infect Genet Evol 30 (2015), 55–58.
94. Taniguchi, S., Maeda, K., Horimoto, T., Masangkay, J.S., Puentespina, R. Jr., Alvarez, J., Eres, E., Cosico, E., Nagata, N., Egawa, K., et al. First isolation and characterization of pteropine orthoreoviruses in fruit bats in the Philippines. Arch Virol 162 (2017), 1529–1539.
95. Takemae, H., Basri, C., Mayasari, N., Tarigan, R., Shimoda, H., Omatsu, T., Supratikno, Pramono, D., Cahyadi, D.D., Kobayashi, R., et al. Isolation of Pteropine orthoreovirus from Pteropus vampyrus in Garut, Indonesia. Virus Genes 54 (2018), 823–827.
96. Singh, H., Shimojima, M., Ngoc, T.C., Quoc Huy, N.V., Chuong, T.X., Le Van, A., Saijo, M., Yang, M., Sugamata, M., Serological evidence of human infection with Pteropine orthoreovirus in Central Vietnam. J Med Virol 87 (2015), 2145–2148.
97. Voon, K., Tan, Y.F., Leong, P.P., Teng, C.L., Gunnasekaran, R., Ujang, K., Chua, K.B., Wang, L.F., Pteropine orthoreovirus infection among out-patients with acute upper respiratory tract infection in Malaysia. J Med Virol 87 (2015), 2149–2153.
98. Yinda, C.K., Ghogomu, S.M., Conceição-Neto, N., Beller, L., Deboutte, W., Vanhulle, E., Maes, P., Van Ranst, M., Matthijnssens, J., Cameroonian fruit bats harbor divergent viruses, including rotavirus H, bastroviruses, and picobirnaviruses using an alternative genetic code. Virus Evol, 4, 2018 vey008-vey008.
99. Geldenhuys, M., Mortlock, M., Weyer, J., Bezuidt, O., Seamark, E.C.J., Kearney, T., Gleasner, C., Erkkila, T.H., Cui, H., Markotter, W., A metagenomic viral discovery approach identifies potential zoonotic and novel mammalian viruses in Neoromicia bats within South Africa. PLoS One, 13, 2018, e0194527.
100. Tse, H., Chan, W.M., Li, K.S., Lau, S.K., Woo, P.C., Yuen, K.Y., Discovery and genomic characterization of a novel bat sapovirus with unusual genomic features and phylogenetic position. PLoS One, 7, 2012, e34987.
101. Wang, J., Moore, N.E., Murray, Z.L., McInnes, K., White, D.J., Tompkins, D.M., Hall, R.J., Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina tuberculata). J Gen Virol 96 (2015), 2442–2452.
102. Kemenesi, G., Dallos, B., Görföl, T., Boldogh, S., Estók, P., Kurucz, K., Kutas, A., Földes, F., Oldal, M., Németh, V., et al. Molecular survey of RNA viruses in Hungarian bats: discovering novel astroviruses, coronaviruses, and caliciviruses. Vector-Borne Zoonotic Dis 14 (2014), 846–855.
103. Waruhiu, C., Ommeh, S., Obanda, V., Agwanda, B., Gakuya, F., Ge, X.-Y., Yang, X.-L., Wu, L.-J., Zohaib, A., Hu, B., et al. Molecular detection of viruses in Kenyan bats and discovery of novel astroviruses, caliciviruses and rotaviruses. Virol Sin 32 (2017), 101–114.
104. Yinda, C.K., Zeller, M., Conceição-Neto, N., Maes, P., Deboutte, W., Beller, L., Heylen, E., Ghogomu, S.M., Van Ranst, M., Matthijnssens, J., Novel highly divergent reassortant bat rotaviruses in Cameroon, without evidence of zoonosis. Sci Rep, 6, 2016, 34209.
105. He, B., Huang, X., Zhang, F., Tan, W., Matthijnssens, J., Qin, S., Xu, L., Zhao, Z., Le, Yang, Wang, Q., et al. Group A rotaviruses in Chinese bats: genetic composition, serology and evidence for bat–to–human transmission and reassortment. J Virol, 91, 2017 pii: e02493-16.
106. He, B., Yang, F., Yang, W., Zhang, Y., Feng, Y., Zhou, J., Xie, J., Feng, Y., Bao, X., Guo, H., et al. Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J Virol 87 (2013), 12357–12366.
107. Le, Yang, Wang, Q., Xu, L., Tu, C., Huang, X., He, B., Detection and characterization of a novel norovirus in bats, China. Virol Sin 33 (2018), 100–103.
108. Wu, Z., Yang, L., Ren, X., He, G., Zhang, J., Yang, J., Qian, Z., Dong, J., Sun, L., Zhu, Y., et al. Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J 10 (2016), 609–620.
109. Kocher, J.F., Lindesmith, L.C., Debbink, K., Beall, A., Mallory, M.L., Yount, B.L., Graham, R.L., Huynh, J., Gates, J.E., Donaldson, E.F., et al. Bat caliciviruses and human noroviruses are antigenically similar and have overlapping histo-blood group antigen binding profiles. mBio, 9, 2018.
110. Tong, S., Li, Y., Rivailler, P., Conrardy, C., Castillo, D.A.A., Chen, L.-M., Recuenco, S., Ellison, J.A., Davis, C.T., York, I.A., et al. A distinct lineage of influenza A virus from bats. Proc Nat Acad Sci U S A, 109, 2012, 4269.
111. Tong, S., Zhu, X., Li, Y., Shi, M., Zhang, J., Bourgeois, M., Yang, H., Chen, X., Recuenco, S., Gomez, J., et al. New world bats harbor diverse influenza A viruses. PLOS Pathog, 9, 2013, e1003657.
112. Moreira, ÉA., Locher, S., Kolesnikova, L., Bolte, H., Aydillo, T., García-Sastre, A., Schwemmle, M., Zimmer, G., Synthetically derived bat influenza A-like viruses reveal a cell type- but not species-specific tropism. Proc Nat Acad Sci U S A, 113, 2016, 12797.
113. Zhou, B., Ma, J., Liu, Q., Bawa, B., Wang, W., Shabman, R.S., Duff, M., Lee, J., Lang, Y., Cao, N., et al. Characterization of uncultivable bat influenza virus using a replicative synthetic virus. PLoS Pathog, 10, 2014, e1004420.
114. Ciminski, K., Thamamongood, T., Zimmer, G., Schwemmle, M., Novel insights into bat influenza A viruses. J Gen Virol 98 (2017), 2393–2400.
115. Guo, W.-P., Lin, X.-D., Wang, W., Tian, J.-H., Cong, M.-L., Zhang, H.-L., Wang, M.-R., Zhou, R.-H., Wang, J.-B., Li, M.-H., et al. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog, 9, 2013, e1003159.
116. Weiss, S., Witkowski, P.T., Auste, B., Nowak, K., Weber, N., Fahr, J., Mombouli, J.-V., Wolfe, N.D., Drexler, J.F., Drosten, C., et al. Hantavirus in bat, Sierra Leone. Emerg Infect Dis 18 (2012), 159–161.
117. Kim, G.R., Lee, Y.T., Park, C.H., A new natural reservoir of hantavirus: isolation of hantaviruses from lung tissues of bats. Arch Virol 134 (1994), 85–95.
118. Sabino-Santos, G. Jr, Maia, F.G.M., Vieira, T.M., de Lara Muylaert, R., Lima, S.M., Gonçalves, C.B., Barroso, P.D., Melo, M.N., Jonsson, C.B., Goodin, D., et al. Evidence of hantavirus infection among bats in Brazil. Am J Trop Med Hyg 93 (2015), 404–406.
119. Sabino-Santos, G. Jr, Maia, F.G.M., Martins, R.B., Gagliardi, T.B., Souza, W.M.D., Muylaert, R.L., Luna, L.K.D.S., Melo, D.M., Cardoso, R.D.S., Barbosa, N.D.S., et al. Natural infection of Neotropical bats with hantavirus in Brazil. Sci Rep, 8, 2018, 9018.
120. de Araujo, J., Thomazelli, L.M., Henriques, D.A., Lautenschalager, D., Ometto, T., Dutra, L.M., Aires, C.C., Favorito, S., Durigon, E.L., Detection of hantavirus in bats from remaining rain forest in Sao Paulo, Brazil. BMC Res Notes, 5, 2012, 690.
121. Xu, B., Liu, L., Huang, X., Ma, H., Zhang, Y., Du, Y., Wang, P., Tang, X., Wang, H., Kang, K., et al. Metagenomic analysis of fever, thrombocytopenia and leukopenia syndrome (FTLS) in Henan Province, China: discovery of a new bunyavirus. PLoS Pathog, 7, 2011, e1002369.
122. McMullan, L.K., Folk, S.M., Kelly, A.J., MacNeil, A., Goldsmith, C.S., Metcalfe, M.G., Batten, B.C., Albarino, C.G., Zaki, S.R., Rollin, P.E., et al. A new phlebovirus associated with severe febrile illness in Missouri. N Engl J Med 367 (2012), 834–841.
123. Mourya, D.T., Yadav, P.D., Basu, A., Shete, A., Patil, D.Y., Zawar, D., Majumdar, T.D., Kokate, P., Sarkale, P., Raut, C.G., et al. Malsoor virus, a novel bat phlebovirus, is closely related to severe fever with thrombocytopenia syndrome virus and heartland virus. J Virol 88 (2014), 3605–3609.
124. Pawan, J.L., Rabies in the vampire bat of Trinidad, with special reference to the clinical course and the latency of infection. Caribb Med J 21 (1959), 137–156.
125. Waterman, J.A., The history of the outbreak of paralytic rabies in Trinidad transmitted by bats to human beings and the lower animals from 1925. Caribb Med J 21 (1959), 1–6.
126. Francis, J.R., McCall, B.J., Hutchinson, P., Powell, J., Vaska, V.L., Nourse, C., Australian bat lyssavirus: implications for public health. Med J Aust 201 (2014), 647–649.
127. Smith, E.C., Blanc, H., Vignuzzi, M., Denison, M.R., Coronaviruses lacking exoribonuclease activity are susceptible to lethal mutagenesis: evidence for proofreading and potential therapeutics. PLoS Pathog, 10, 2013.
128. Denison, M.R., Graham, R.L., Donaldson, E.F., Eckerle, L.D., Baric, R.S., Coronaviruses: an RNA proofreading machine regulates replication fidelity and diversity. RNA Biol 8 (2011), 270–279.
129. Hu, B., Zeng, L.P., Yang, X.L., Ge, X.Y., Zhang, W., Li, B., Xie, J.Z., Shen, X.R., Zhang, Y.Z., Wang, N., et al. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathog, 13, 2017, e1006698 A very detailed study to show that all building blocks of SARS-CoV are present among a diverse group of CoVs in the same cave.
130. Huang, C., Liu, W.J., Xu, W., Jin, T., Zhao, Y., Song, J., Shi, Y., Ji, W., Jia, H., Zhou, Y., et al. A bat-derived putative cross-family recombinant coronavirus with a reovirus gene. PLoS Pathog, 12, 2016, e1005883 An important finding demonstrating that CoVs are highly active in recombination, even with viruses outside the coronavirus family.
131. Obameso, J.O., Li, H., Jia, H., Han, M., Zhu, S., Huang, C., Zhao, Y., Zhao, M., Bai, Y., Yuan, F., et al. The persistent prevalence and evolution of cross-family recombinant coronavirus GCCDC1 among a bat population: a two-year follow-up. Sci China Life Sci 60 (2017), 1357–1363.
132. Lau, S.K.P., Chan, J.F.W., Coronaviruses: emerging and re-emerging pathogens in humans and animals. Virol J, 12, 2015, 209.
133. Saif, L.J., Animal coronaviruses: what can they teach us about the severe acute respiratory syndrome?. Rev Sci Tech 23 (2004), 643–660.
134. Zhou, P., Tachedjian, M., Wynne, J.W., Boyd, V., Cui, J., Smith, I., Cowled, C., Ng, J.H., Mok, L., Michalski, W.P., et al. Contraction of the type I IFN locus and unusual constitutive expression of IFN-alpha in bats. Proc Natl Acad Sci U S A 113 (2016), 2696–2701.
135. Wynne, J.W., Shiell, B.J., Marsh, G.A., Boyd, V., Harper, J.A., Heesom, K., Monaghan, P., Zhou, P., Payne, J., Klein, R., et al. Proteomics informed by transcriptomics reveals Hendra virus sensitizes bat cells to TRAIL-mediated apoptosis. Genome Biol, 15, 2014, 532.
136. Ahn, M., Cui, J., Irving, A.T., Wang, L.F., Unique loss of the PYHIN gene family in bats amongst mammals: implications for inflammasome sensing. Sci Rep, 6, 2016, 21722.
137. Xie, J., Li, Y., Shen, X., Goh, G., Zhu, Y., Cui, J., Wang, L.F., Shi, Z.L., Zhou, P., Dampened STING-dependent interferon activation in bats. Cell Host Microbe 23 (2018), 297–301 e294.
138. Pavlovich, S.S., Lovett, S.P., Koroleva, G., Guito, J.C., Arnold, C.E., Nagle, E.R., Kulcsar, K., Lee, A., Thibaud-Nissen, F., Hume, A.J., et al. The Egyptian rousette genome reveals unexpected features of bat antiviral immunity. Cell 173 (2018), 1098–1110 e1018.